Department of Degenerative Neurological Diseases, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan.
Division of Clinical Genetics, Osaka University Graduate School of Medicine, Suita, Osaka, Japan.
Brain. 2020 Jun 1;143(6):1811-1825. doi: 10.1093/brain/awaa115.
The polyglutamine (polyQ) diseases are a group of inherited neurodegenerative diseases that include Huntington's disease, various spinocerebellar ataxias, spinal and bulbar muscular atrophy, and dentatorubral pallidoluysian atrophy. They are caused by the abnormal expansion of a CAG repeat coding for the polyQ stretch in the causative gene of each disease. The expanded polyQ stretches trigger abnormal β-sheet conformational transition and oligomerization followed by aggregation of the polyQ proteins in the affected neurons, leading to neuronal toxicity and neurodegeneration. Disease-modifying therapies that attenuate both symptoms and molecular pathogenesis of polyQ diseases remain an unmet clinical need. Here we identified arginine, a chemical chaperone that facilitates proper protein folding, as a novel compound that targets the upstream processes of polyQ protein aggregation by stabilizing the polyQ protein conformation. We first screened representative chemical chaperones using an in vitro polyQ aggregation assay, and identified arginine as a potent polyQ aggregation inhibitor. Our in vitro and cellular assays revealed that arginine exerts its anti-aggregation property by inhibiting the toxic β-sheet conformational transition and oligomerization of polyQ proteins before the formation of insoluble aggregates. Arginine exhibited therapeutic effects on neurological symptoms and protein aggregation pathology in Caenorhabditis elegans, Drosophila, and two different mouse models of polyQ diseases. Arginine was also effective in a polyQ mouse model when administered after symptom onset. As arginine has been safely used for urea cycle defects and for mitochondrial myopathy, encephalopathy, lactic acid and stroke syndrome patients, and efficiently crosses the blood-brain barrier, a drug-repositioning approach for arginine would enable prompt clinical application as a promising disease-modifier drug for the polyQ diseases.
多聚谷氨酰胺(polyQ)疾病是一组遗传性神经退行性疾病,包括亨廷顿病、各种脊髓小脑共济失调、脊髓和延髓肌肉萎缩症,以及齿状核红核苍白球路易体萎缩症。它们是由每个疾病的致病基因中 CAG 重复编码的多聚 Q 延伸的异常扩展引起的。扩展的多聚 Q 延伸引发异常的β-折叠构象转变和寡聚化,随后多聚 Q 蛋白在受影响的神经元中聚集,导致神经元毒性和神经退行性变。减轻多聚 Q 疾病的症状和分子发病机制的疾病修饰疗法仍然是未满足的临床需求。在这里,我们确定精氨酸,一种促进正确蛋白质折叠的化学伴侣,是一种新型化合物,通过稳定多聚 Q 蛋白构象来靶向多聚 Q 蛋白聚集的上游过程。我们首先使用体外多聚 Q 聚集测定法筛选代表性的化学伴侣,鉴定精氨酸是一种有效的多聚 Q 聚集抑制剂。我们的体外和细胞测定显示,精氨酸通过在不溶性聚集体形成之前抑制多聚 Q 蛋白的毒性β-折叠构象转变和寡聚化来发挥其抗聚集特性。精氨酸在秀丽隐杆线虫、果蝇和两种不同的多聚 Q 疾病小鼠模型中表现出对神经症状和蛋白质聚集病理学的治疗作用。精氨酸在症状出现后给药时对多聚 Q 小鼠模型也有效。由于精氨酸已安全用于尿素循环缺陷和线粒体肌病、脑病、乳酸酸中毒和中风综合征患者,并且能够有效地穿过血脑屏障,因此对精氨酸进行药物重新定位的方法将使它能够作为一种有前途的多聚 Q 疾病疾病修饰药物迅速应用于临床。